Article
Reference
Mechanosensitive membrane probes: push-pull papillons
HUMENIUK, Heorhii, et al.
Abstract
Design, synthesis and evaluation of push-pull N,N′-diphenyl-dihydrodibenzo[a,c]phenazines are reported. Consistent with theoretical predictions, donors and acceptors attached to the bent mechanophore are shown to shift absorption maxima to either red or blue, depending on their positioning in the chromophore. Redshifted excitation of push-pull fluorophores is reflected in redshifted emission of both bent and planar excited states. The intensity ratios of the dual emission in more and less polar solvents imply that excited-state (ES) planarization decelerates with increasing fluorophore macrodipole, presumably due to attraction between the wings of closed papillons. ES planarization of highly polarisable papillons is not observed in lipid bilayer membranes. All push-pull papillon amphiphiles excel with aggregation-induced emission (AIE) from bent ES as micelles in water and mechanosensitivity in viscous solvents.
They are not solvatochromic and only weakly fluorescent (QY < 4%).
HUMENIUK, Heorhii, et al. Mechanosensitive membrane probes: push-pull papillons.
Supramolecular Chemistry, 2020, vol. 32, no. 2, p. 106-111
DOI : 10.1080/10610278.2019.1702193
Available at:
http://archive-ouverte.unige.ch/unige:131618
Disclaimer: layout of this document may differ from the published version.
Mechanosensitive Membrane Probes: Push-Pull Papillons‡
Heorhii V. Humeniuk,a Giuseppe Licari,a,b Eric Vauthey,a Naomi Sakaia and Stefan Matile*,a
a School of Chemistry and Biochemistry, University of Geneva, Geneva, Switzerland
b Current address: NIH Center for Macromolecular Modeling and Bioinformatics, Beckman Institute for Advanced
Science and Technology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, United States
stefan.matile@unige.ch
‡Invited contribution to the special issue on ISMSC-14, the 14th International Symposium on Macrocyclic and Supramolecular Chemistry, Lecce, Italy, June 2019
Design, synthesis and evaluation of push-pull N,N′-diphenyl-dihydrodibenzo[a,c]phenazines are reported. Consistent with theoretical predictions, donors and acceptors attached to the bent mechanophore are shown to shift absorption maxima to either red or blue, depending on their positioning in the chromophore. Redshifted excitation of push-pull fluorophores is reflected in redshifted emission of both bent and planar excited states. The intensity ratios of the dual emission in more and less polar solvents imply that excited-state (ES) planarization decelerates with increasing fluorophore macrodipole, presumably due to attraction between the wings of closed papillons. ES planarization of highly polarizable papillons is not observed in lipid bilayer membranes. All push- pull papillon amphiphiles excel with aggregation-induced emission (AIE) from bent ES as micelles in water and mechanosensitivity in viscous solvents. They are not solvatochromic and only weakly fluorescent (QY < 4%).
Keywords: Mechanochemistry; bent aromatics; fluorescent probes; lipid bilayer membranes; push–pull systems
Introduction
Although membrane tension is expected to play a central role in many biological processes (1), fluorescent probes to image this force in living cells remain elusive. To change this situation, we have introduced fluorescent membrane probes (2–4) that operate with a combination of planarization and polarization in the ground state (GS) (5). Their unprecedented, uniform response to membrane tension in all tested cells is revealing tension-induced membrane domain assembly and disassembly as a general mode to mediate biological function (6), including signal transduction (7). Operating in equilibrium in the GS, planarizable push-pull Flipper-TR® probes differ from other membrane probes (2–4) that, except for the most recent polyimine dynamers (4), operate off-equilibrium in the excited state (ES) and thus report on kinetics, i.e., viscosity, rather than sterics. Like all other mechanosensitive membrane probes (2–4), however, Flipper-TR® probes operate with twisted fluorophores (5).
To move from twisting to bending (8), molecular papillons have been recently introduced (Figure 1a) (9). Bent N,N′-diphenyl-dihydrodibenzo[a,c]phenazine (10) amphiphiles have been shown to
report on the order of lipid bilayer membranes by mechanosensitive planarization in the excited state.
Because they operate -equilibrium, papillons in micellar states and liquid- and solid-ordered (Lo, So) membranes emit from the bent form, whereas those in liquid-disordered (Ld) and bulk membranes emit from the planar form (Figure 1d–f). The resulting shifts in emission are so large that they cover the full visible range. The emitted white light is, however, ratiometrically encoded to report on the order of the membranes (9), which has been shown to change with membrane tension (6).
Considering that the so far unique operational tension probes act by a combination of planarization and polarization, it was of interest to see how polarization would influence the performance of the bent rather than twisted papillon mechanophores. In the following, we describe the design, synthesis and evaluation of push-pull papillons.
Results and Discussion
Push-pull dipoles in dihydrodibenzo[a,c]phenazines can be oriented from the phenylene to the phenanthrylene of the central heterocycle (Figures 1b, S10) and from the phenanthrylene to the phenylene side (Figures 1c, S10). Computational studies of the permanent dipole moments as well as the frontier molecular orbitals (Figures 1g-k, S11, Table S5) suggested that only the former would afford operational push–pull fluorophores. For a representative system with cyano acceptors on the phenanthrylene and methoxy donors on the phenylene side (Figure 1b), electron density in the HOMO localized clearly on the donor side, including the central 1,4-dihydropyrazine heterocycle (Figure 1g).
Excitation to the LUMO caused the complete intramolecular charge transfer from donors to acceptors that is characteristic for operational push–pull fluorophores (Figure 1h, 90% contribution to the transition). In clear contrast, two cyano acceptors on the phenylene side (Figure 1c) localized the HOMO mainly in the phenanthrene ring with only partial extension into the 1,4-dihydropyrazine (Figure 1i). Moreover, the LUMO with density near the acceptors (Figure 1j, 66% contribution)
occurred nearly degenerate together with LUMO+1 with density nearer the donor than the acceptor (Figure 1k, 14%).
Figure 1. a) Original papillon probes differentiate between d) disordered and e) ordered lipid bilayer membranes, f) water and a) lipophilic solvents by emission from bent (purple) and planar (yellow) excited states. b) Normal and c) reverse push-pull papillons are expected to absorb at longer and shorter wavelength compared to original papillons, respectively: g-k) DFT (CAM-B3LYP/6–
31+G(d,p)) calculations of g) HOMO and h) LUMO orbitals of normal push-pull papillon with two cyano acceptors (blue arrows) and three methoxy donors (red arrows (one omitted for clarity), b; see Scheme 1) and i) HOMO, j) LUMO and k) LUMO+1 orbitals of the complementary reverse push-pull papillon (c).
The N,N′-diphenyl-dihydrodibenzo[a,c]phenazine amphiphiles 1–6 were synthesized to elaborate on these expectations (Scheme 1). The synthesis of push-pull papillon 1 was accomplished in five steps from 9,10-phenanthrenequinone 7. Free-radical bromination of 7 afforded 8, which was subsequently subjected to reductive amination by first imine formation with p-anisidine and then reduction with hydrazine hydrate on Pd/C. Cu-catalyzed Ullmann domino reaction of diamine 9 with iodophenyl 10 gave papillon 11. Nucleophilic aromatic substitution with CuCN afforded the push- pull scaffold
Scheme 1. a) Br2, BPO, nitrobenzene, 110 oC, overnight, 57%; b) 1. aniline, pyridine, TiCl4, CH2Cl2, RT, overnight, 2. hydrazine hydrate, Pd/C, THF, RT, 2 h, 31%; c) K2CO3, Cu(OTf)2, 1,2,4- trichlorobenzene, 210 oC, overnight, 5%; d) CuCN, NMP, 150 oC, overnight, 8%; e) Me3SnOH, DCE, reflux, 3 h, 49%.
12. The desired amphiphile 1 was obtained by mild basic ester hydrolysis with Me3SnOH. Papillons 2–4 were prepared analogously (Scheme S1–S4), whereas 5 and 6 were synthesized following previously reported procedures (9).
N N R2 R2
O OH O
2: R1 = H, R2 = CN 3: R1 = CN, R2 = OMe 4: R1 = CN, R2 = H 5: R1 = H, R2 = H 6: R1 = H, R2 = OMe O
O Br
Br O
O
R1
R1 N
N NC NC
O OR O
OMe
OMe 12: R = OEt 1: R = H N
N Br Br
O OR O
OMe
OMe
NH NH Br Br
OMe
OMe
O OR O
I
7 8 9
11 10
a)
c) d) e)
b)
Toluene was used as representative hydrophobic solvent because solubilities of the papillon amphiphiles in apolar alkanes such as cyclohexane were insufficient. As a monomer in toluene, the original papillon 5 absorbed at labs=355 nm (Figure 2a, green, solid). The absorption of push-pull papillon 1 at labs=422 nm was Dlabs=+67 nm redshifted (Figure 2a, blue, solid). The reverse push- pull papillon 3 absorbed at labs=318 nm, that is Dlabs= –37 nm blueshifted (Figure 2a, red, solid).
These complementary shifts were as expected from theory (Figure 1; 1: labs,calc=384 nm, 3:
labs,calc=322 nm, Table S5). Weakening of the push-pull systems in 2, 4 and 6 weakened the batho- and hypsochromic effects correspondingly (Figure 2a, dotted, magenta and dashed, respectively). The absorption maxima of all papillons were almost insensitive to their environment, including solvent polarity, micelles and phases of lipid bilayer membranes (Figures 3a-c). This lack of responsiveness demonstrated that planarization of bent chromophores does not occur in the GS.
As monomers in organic solvents, the original papillon 5 emitted with a quantum yield of 14%
(9). With most quantum yields below 1%, the fluorescence of the new push-pull papillons was much weaker (Table S1, S2).
The original papillon 5 excels with ratiometric dual emission from bent and planar ES, characterized by the intensity ratio Ib/p (9). At one extreme, as micelles in water (Figure 1f), 5 emits almost exclusively blue light at lem=459 nm because the tight packing of the closed papillons inhibits their opening in the ES (Figure 3d, magenta). At the other extreme, monomers in toluene show mostly orange fluorescence at lem=614 nm because papillon opening in the ES is faster than emission from the bent ES (Figures 2b, solid, green; 3d, black).
The emission maxima of the only partially polarized push-pull papillon 2 in toluene appeared at lem=689 nm and lem=565 nm with Ib/p = 0.3 (Figure 2b, dotted). Papillon 2 thus roughly reproduced the characteristics of original 5 with a redshift of Dlem=+75 nm for the dominant emission from the planar ES at lem=689 nm. This redshift in emission was consistent with expectations and nicely reproduced the redshift in excitation (Figure 2a, dotted).
Figure 2. Normalized absorption (a) and emission spectra (b) of 1 (blue), 2 (black, dotted), 3 (red), 4 (magenta), 5 (green) and 6 (black, dashed) in toluene.
The fully polarized push-pull papillon 1 showed a very broad emission maximum from 550 – 800 nm (Figures 2b, blue solid; 3e, black, dotted). Two flat peaks of almost equal intensity at lem=682 nm and lem=608 nm suggested that push-pull papillon 1 opens up only partially in the ES (i.e. Ib/p = 0.9). The validity of this interpretation was confirmed by increasingly hypsochromic emission with increasing viscosity to end up with exclusive lem=601 nm in pure glycerol (i.e. Ib/p > 20, Figure S7, Table S3) and with aggregation-induced emission (AIE) (11) from micelles in water (Figure 3e, magenta).
The reverse push-pull papillon 3 emitted in toluene at lem=616 nm (Figure 2b, red, solid).
Although nearly overlapping with emission from the bent ES of push-pull papillon 1, this emission was attributed to complete ES planarization (Ib/p < 0.1). Emission from closed reverse push-pull papillon 3 in glycerol (Figure S7) or AIE from micelles in water occurred more blueshifted at lem=504 nm (Figure 3f, magenta).
The original papillon 5 has been shown to emit ratiometrically encoded white light from lipid bilayer membranes (9). In solid-ordered (So) membranes of large unilamellar vesicles (LUVs) composed of DPPC at 25 ºC, emission from bent ES dominates emission from planar ES clearly (Figure 3a, blue, solid). Emission from So DPPC LUVs approached the AIE from micellar aggregates
of completely closed papillons in water (Figure 3d, magenta). In Ld DPPC LUVs at 55 ºC, emission from open papillons dominated (Figure 3a, red, solid), although not as clearly as in toluene (Figure 3d, black). In Ld DOPC LUVs at 25 ºC, emission from open papillons remained significant (Figure 3a, blue, dashed). This dual emission covering the entire visible range provided access to quantitative ratiometric imaging of the order of lipid bilayer membranes.
Figure 3. a-c) Normalized excitation (left) and emission spectra (right) of a) 5, b) 1 and c) 3 in DPPC LUVs (solid), DOPC LUVs (dashed) at 55 °C (red) and 25 °C (blue). d-f) Emission spectra of d) 5, e) 1 and f) 3 in Tris buffer (magenta) and toluene (black).
The redshifted excitation maximum of push-pull papillon 1 was insensitive to the surrounding lipid bilayer membrane (Figure 3b). This insensitivity was as with original papillon 5 (Figure 3a) and excluded the mechanosensitvity in the GS known from flipper probes (5). Also almost independent of the surrounding lipid bilayer membrane, the emission of push-pull papillon 1 (Figure 3b) was similar to AIE from micelles in water (Figure 3e, magenta). This behavior was contrary to original 5 and indicated that either ES planarization does not occur with 1 in membranes, or 1 does not partition into the membrane. The former would not surprise considering that ES planarization was only partial already in toluene (Figure 3e, black).
Emission of the reverse push-pull papillon 3 from So DPPC LUVs (Figure 3c, blue, solid) was almost the same as AIE from closed papillons in micelles in water (Figure 3f, dashed). This similarity suggested that in So membranes, reverse papillon 3 emits from bent ES. Emission from Ld DPPC LUVs at 55 ºC (Figure 3c, red, solid) was almost as in toluene (Figure 3f, black), thus supporting emission from planar ES in “hot” Ld DPPC membranes. In Ld DOPC LUVs at 25 ºC, broad emission between the maxima of closed and open papillons was consistent with partial planarization in the excited state (Figure 3a, blue, dashed).
Both emissions of reverse push-pull papillon 3 were redshifted compared to original 5 (Figure 3a vs 3c). However, the redshift of the bent ES (467 to 515 nm) was larger than that of the planar ES (587 to 592 nm), which added up to a reduced mechanosensitivty of 3 (Dlem=77 nm, Ib/p=1.6) compared to 5 (Dlem=120 nm, Ib/p=3.4, Figures 3a, c).
Conclusions
Fascinated by the potential of the bent papillons as fluorescent probes to image physical forces in living cells, the objective of this study was to design, synthesize and evaluate push-pull papillons. For this purpose, push-pull papillons 1 and 2 and reverse push-pull papillons 3 and 4 were prepared. They show the predicted red- and blueshifts in absorption. For both, blueshifted emission from bent ES occurs from micelles in water, from monomers in viscous glycerol, and from So lipid bilayer membranes. Only partially redshifted emission in organic solvents and no significant redshifts in Ld
membranes demonstrates that ES planarization of push-pull papillons 1 is hindered, possibly due to dipole attraction between the two wings in the closed papillons. Redshifted emission from planar ES of monomers in organic solvents as well as Ld membranes was found for reverse push-pull papillons 3. However, they are less mechanosensitive than the original 5 because the redshift of emission from bent ES exceeds that from planar ES. These results demonstrate that both push-pull and reverse push- pull papillons are significant with regard to fundamental concepts but not promising as mechanophores
in practice. This conclusion is further supported by their nearly negligible fluorescence quantum yields.
Supporting Information Experimental details.
Acknowledgements
We thank the NMR and the MS platforms for services, and the University of Geneva, the Swiss National Centre of Competence in Research (NCCR) Chemical Biology, the NCCR Molecular Systems Engineering and the Swiss NSF for financial support.
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